Will chemical defenses become more effective against specialist herbivores under elevated CO2?

Elevated atmospheric CO2 is known to affect plant-insect herbivore interactions. Elevated CO2 causes leaf nitrogen to decrease, the ostensible cause of herbivore compensatory feeding. CO2 may also affect herbivore consumption by altering chemical defenses via changes in plant hormones. We considered the effects of elevated CO2, in conjunction with soil fertility and damage (simulated herbivory), on glucosinolate concentrations of mustard (Brassica nigra) and collard (B. oleracea var. acephala) and the effects of leaf nitrogen and glucosinolate groups on specialist Pieris rapae consumption. Elevated CO2 affected B. oleracea but not B. nigra glucosinolates; responses to soil fertility and damage were also species-specific. Soil fertility and damage also affected B. oleracea glucosinolates differently under elevated CO2. Glucosinolates did not affect P. rapae consumption at either CO2 concentration in B. nigra, but had CO2-specific effects on consumption in B. oleracea. At ambient CO2, leaf nitrogen had strong effects on glucosinolate concentrations and P. rapae consumption but only gluconasturtiin was a feeding stimulant. At elevated CO2, direct effects of leaf nitrogen were weaker, but glucosinolates had stronger effects on consumption. Gluconasturtiin and aliphatic glucosinolates were feeding stimulants and indole glucosinolates were feeding deterrents. These results do not support the compensatory feeding hypothesis as the sole driver of changes in P. rapae consumption under elevated CO2. Support for hormone-mediated CO2 response (HMCR) was mixed; it explained few treatment effects on constitutive or induced glucosinolates, but did explain patterns in SEMs. Further, the novel feeding deterrent effect of indole glucosinolates under elevated CO2 in B. oleracae underscores the importance of defensive chemistry in CO2 response. We speculate that P. rapae indole glucosinolate detoxification mechanisms may have been overwhelmed under elevated CO2 forcing slowed consumption. Specialists may have to contend with hosts with poorer nutritional quality and more effective chemical defenses under elevated CO2.

Elevated CO2 increases constitutive phenolics and trichomes, but decreases inducibility of phenolics in Brassica rapa (Brassicaceae).

Increasing global atmospheric CO2 has been shown to affect important plant traits, including constitutive levels of defensive compounds. However, little is known about the effects of elevated CO2 on the inducibility of chemical defenses or on plant mechanical defenses. We grew Brassica rapa (oilseed rape) under ambient and elevated CO2 to determine the effects of elevated CO2 on constitutive levels and inducibility of carbon-based phenolic compounds, and on constitutive trichome densities. Trichome density increased by 57% under elevated CO2. Constitutive levels of simple, complex, and total phenolics also increased under elevated CO2, but inducibility of each decreased. Induction of simple phenolics occurred only under ambient CO2. Although induction of complex and total phenolics occurred under both ambient and elevated CO2, the damage-induced increases were 64% and 75% smaller, respectively, under elevated CO2. Constitutive phenolic levels were positively correlated with leaf C:N ratio, and inducibility was positively correlated with leaf N and negatively correlated with leaf C:N ratio, as would be expected if inducibility were constrained by nitrogen availability under elevated CO2. We conclude that B. rapa is likely to exhibit higher constitutive levels of both chemical and mechanical defenses in the future, but is also likely to be less able to respond to herbivore damage by inducing phenolic defenses. To our knowledge, this is only the second study to report a negative effect of elevated CO2 on the inducibility of any plant defense.

Effects of elevated atmospheric CO2 on the nutritional ecology of C3 and C4 grass-feeding caterpillars.

It is plausible that the nutritional quality of C3 plants will decline more under elevated atmospheric CO2 than will the nutritional quality of C4 plants, causing herbivorous insects to increase their feeding on C3 plants relative to C4 plants. We tested this hypothesis with a C3 and C4 grass and two caterpillar species with different diet breadths. Lolium multiflorum (C3) and Bouteloua curtipendula (C4) were grown in outdoor open top chambers at ambient (370 ppm) or elevated (740 ppm) CO2. Bioassays compared the performance and digestive efficiencies of Pseudaletia unipuncta (a grass-specialist noctuid) and Spodoptera frugiperda (a generalist noctuid). As expected, the nutritional quality of L. multiflorum changed to a greater extent than did that of B. curtipendula when grown in elevated CO2; levels of protein (considered growth limiting) declined in the C3 grass, while levels of carbohydrates (sugar, starch and fructan) increased. However, neither insect species increased its feeding rate on the C3 grass to compensate for its lower nutritional quality when grown in an elevated CO2 atmosphere. Consumption rates of P. unipuncta and S. frugiperda were higher on the C3 grass than the C4 grass, the opposite of the result expected for a compensatory response to the lower nutritional quality of the C4 grass. Although our results do not support the hypothesis that grass-specialist insects compensate for lower nutritional quality by increasing their consumption rates more than do generalist insects, the performance of the specialist was greater than that of the generalist on each grass species and at both CO2 levels. Mechanisms other than compensatory feeding, such as increased nutrient assimilation efficiency, appear to determine the relative performance of these herbivores. Our results also provide further evidence against the hypothesis that C4 grasses would be avoided by insect herbivores because a large fraction of their nutrients is unavailable to herbivores. Instead, our results are consistent with the hypothesis that C4 grasses are poorer host plants primarily because of their lower nutrient levels, higher fiber levels, and greater toughness.

Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality.

The increasing CO2 concentration in Earth's atmosphere is expected to cause a greater decline in the nutritional quality of C3 than C4 plants. As a compensatory response, herbivorous insects may increase their feeding disproportionately on C3 plants. These hypotheses were tested by growing the grasses Lolium multiflorum C3) and Bouteloua curtipendula C4) at ambient (370 ppm) and elevated (740 ppm) CO2 levels in open top chambers in the field, and comparing the growth and digestive efficiencies of the generalist grasshopper Melanoplus sanguinipes on each of the four plant x CO2 treatment combinations. As expected, the nutritional quality of the C3 grass declined to a greater extent than did that of the C4 grass at elevated CO2; protein levels declined in the C3 grass, while levels of carbohydrates (sugar, fructan and starch) increased. However, M. sanguinipes did not significantly increase its consumption rate to compensate for the lower nutritional quality of the C3 grass grown under elevated CO2. Instead, these grasshoppers appear to use post-ingestive mechanisms to maintain their growth rates on the C3 grass under elevated CO2. Consumption rates of the C3 and C4 grasses were also similar, demonstrating a lack of compensatory feeding on the C4 grass. We also examined the relative efficiencies of nutrient utilization from a C3 and C4 grass by M. sanguinipes to test the basis for the C4 plant avoidance hypothesis. Contrary to this hypothesis, neither protein nor sugar was digested with a lower efficiency from the C4 grass than from the C3 grass. A novel finding of this study is that fructan, a potentially large carbohydrate source in C3 grasses, is utilized by grasshoppers. Based on the higher nutrient levels in the C3 grass and the better growth performance of M. sanguinipes on this grass at both CO2 levels, we conclude that C3 grasses are likely to remain better host plants than C4 grasses in future CO2 conditions.

PREDICTING HOST RANGE EVOLUTION: COLONIZATION OF CORONILLA VARIA BY COLIAS PHILODICE (LEPIDOPTERA: PIERIDAE).

Extensive sympatry is currently arising between the common sulfur butterfly, Colias philodice Latreille (Lepidoptera: Pieridae) and a potential leguminous host plant, Coronilla varia (L.). In laboratory trials, larval surviviorship and growth were higher on the primary host, Medicago sativa (L.), than on the nonhost C. varia. However, because females reared from C. varia were on average more fecund than females reared from M. sativa, fitness on C. varia (approximately as survivorship times fecundity) was commensurate with fitness on M. sativa. Thus, it is predicted that selection would favor oviposition on C. varia, if such behavior were to arise. In addition, significant among-family variation exists for several measures of larval performance on both C. varia and M. sativa, indicating that C. philodice can potentially respond to selection for increased performance on each species. Moreover, larval performance was significantly positively correlated across these species, suggesting that selection for increased performance on each species will facilitate, not constrain, evolution of increased performance on the other. It is concluded that behavioral rather than physiological barriers currently account for the absence of C. philodice from C. varia and that, if such barriers are overcome, C. philodice will expand its host plant range to include C. varia.

Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant anti-herbivore chemistry.

Feeding efficiencies of ultimate instar larvae of two polyphagous tree-feeding Lepidoptera, Malacosoma disstria (Lasiocampidae) and Orgyia leucostigma (Liparidae), were measured on artificial diets containing from 0% to 8% tannic acid. Relative growth rate (RGR) of O. leucostigma was not affected by up to 8% tannic acid, suggesting that O. leucostigma has evolved an effective counteradaptation to hydrolyzable tannins. In contrast, as little as 0.5% tannic acid caused a significant reduction in RGR of M. disstria, due both to reduced efficiency of conversion of digested food (ECD) and reduced relative consumption rate (RCR), and caused a significant increase in mortality during the pupal stage. Moreover, when reared from hatching on tannin-containing diets, no M. disstria larvae survived past the fourth instar.Although tannins are commonly referred to as "digestibility-reducing substances", tannic acid did not reduce the ability of M. disstria or O. leucostigma larvae to digest either the whole diet or nitrogen contained in the diet. For M. disstria, tannic acid acts as a toxin and a feeding deterrent, but not as a digestibility-reducing substance. Growing evidence that tannins commonly act as toxins warrants a reassessment of their role in anti-herbivore chemistry.